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Metabolic Mechanisms for the Evolution of Stable Symbiosis

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Metabolic Mechanisms for the Evolution of Stable Symbiosis Metabolic mechanisms for the evolution of stable symbiosis Megan Elisabeth Stig Sørensen A thesis submitted for the degree of Doctor of Philosophy University of Sheffield Department of Animal and Plant Sciences September 2019 2 Abstract Endosymbiosis involves the merger of once independent organisms; this evolutionary transition has defined the evolutionary history of eukaryotes and continues to underpin the function of a wide range of ecosystems. Endosymbioses are evolutionarily dynamic because the inherent conflict between the self-interest of the partners make the breakdown of the interaction ever-likely and this is exacerbated by the environmental context dependence of the benefits of symbiosis. This necessitates selection for partner switching, which can reshuffle the genetic identities of symbiotic partnerships and so rescue symbioses from cheater-induced extinction and enable rapid adaptation to environmental change. However, the mechanisms of partner-specificity, that underlie the potential for partner switching, are unknown. Here I report the metabolic mechanisms that control partner specificity within the tractable microbial photosymbiosis between Paramecium bursaria and Chlorella. I have found that metabolic function, and not genetic identity, enables partner-switching, but that genetic variation plays an important role in maintaining variation in symbiotic phenotype. In addition, I observed that symbiont stress-responses played an important role in partner specificity, and that alleviating symbiont stress responses may be an important strategy of generalist host genotypes. Furthermore, I have used experimental evolution to show that a novel, initially non-beneficial association can rapidly evolve to become a beneficial symbiosis. These results demonstrate that partner integration is defined by metabolic compatibility and that initially maladapted host- symbiont pairings can rapidly evolve to overcome their lack of co-adaptation through alterations to metabolism and symbiont regulation. Understanding the process of novel partner integration and partner switching is crucial if we are to understand how new symbioses originate and stabilise. Moreover, mechanistic knowledge of partner switching is required to mitigate the breakdown of symbioses performing important ecosystem functions driven by environmental change, such as in coral reefs. 3 List of Contents Abstract 3 List of Figures 6 List of Tables 8 Acknowledgements 9 Declaration 10 Chapter 1 – Introduction 11 1.1 The Organelles 12 1.2 Secondary Endosymbioses 14 1.3 The parasitism-mutualism continuum 15 1.4 Evolution of partner dependency 17 1.5 Conflict avoidance 19 1.6 Ecology and Physiology of the P. bursaria – Chlorella endosymbiosis 20 1.7 Genetics of the P. bursaria – Chlorella endosymbiosis 26 1.8 Thesis Outline 29 Chapter 2 – Comparison of independent evolutionary origins reveals both convergence and divergence in the metabolic mechanisms of symbiosis 31 2.1 Introduction 31 2.2 Materials and Methods 33 2.3 Results 39 2.4 Discussion 51 2.5 Supplementary Figures 56 2.6 Supplementary Results 61 Chapter 3 – Light-dependent stress-responses underlie host-symbiont genotypic specificity in a photosymbiosis 62 3.1 Introduction 62 3.2 Materials & Methods 65 3.3 Results 68 3.4 Discussion 81 3.5 Supplementary Figures 87 3.6 Supplementary Tables 91 4 Chapter 4 – A novel host-symbiont interaction can rapidly evolve to become a beneficial symbiosis 93 4.1 Introduction 93 4.2 Materials and Methods 95 4.3 Results 98 4.4 Discussion 105 4.5 Supplementary Tables 110 Chapter 5 – Discussion 114 5.1 Stress and symbiosis 115 5.2 Partner Switching 116 5.3 Rapid evolution enables the establishment of symbiosis 118 5.4 Applications of endosymbiosis research 119 5.5 Future-directions 120 5.6 In conclusion 121 Appendix A – The review paper linked to Chapter 1 123 Appendix B – Statistical outputs for Chapter 2 131 Appendix C – Statistical outputs for Chapter 3 134 Appendix D – Statistical outputs for Chapter 4 137 Bibliography 139 5 List of Figures 1.1 Diagrammatic representation of the fitness interactions within endosymbioses 16 1.2. Diagrammatic representation of the P. bursaria - Chlorella endosymbiosis 22 1.3. The consequence of symbiosis for each partner 25 2.1. Correlated metabolite enrichment for the 186b and HA1 P. bursaria and Chlorella strains over time 40 2.2. Fitness of the native and non-native host-symbiont pairings relative to isogenic symbiont-free hosts 44 2.3. Difference in Chlorella global metabolism between strains across light conditions 45 2.4. Difference in P. bursaria global metabolism between strains across light conditions 48 2.5. Photophysiology measurements for the native and non-native host-symbiont pairings 51 S2.1. PCR result of the HA1 and 186b Chlorella strains 56 S2.2. Schematic pathways diagram of nitrogen enrichment in the arginine amino acid metabolism of the Chlorella metabolic fraction 57 S2.3. Schematic pathways diagram of nitrogen enrichment in other aspects of amino acid metabolism in the Chlorella metabolic fraction 58 S2.4. Schematic pathways diagram of nitrogen enrichment in purine metabolism in the Chlorella metabolic fraction 59 S2.5. The interaction of light intensity and strain identity on the 13C enrichment profile of carbohydrate metabolites from the P. bursaria fraction. 60 3.1. Conceptual diagrams of potential outcomes when comparing native and non-native host-symbiont pairings 64 3.2. Initial growth rates of the host-symbiont pairings across a light gradient 69 3.3. Symbiont load of the host-symbiont pairings across a light gradient 70 3.4. The clustering of the metabolic fractions by light 72 3.5. Clustering patterns of the Chlorella metabolic fraction subset by host-genotype 73 6 3.6. Differences in the Chlorella metabolism between symbiont genotypes at multiple light levels within the 186b P. bursaria host 75 3.7. Relative abundances of dark-stress associated metabolites across host genotypes in the dark 80 3.8. Relative abundances of a high-light stress associated metabolite across host genotypes and across light levels 81 S3.1. PCR confirmation of symbiont-genotype within the reciprocal cross infections 87 S3.2. The clustering of the metabolic fractions by light in PCA plots 88 S3.3. Separation by symbiont-genotype within the 186b host subset of the Chlorella metabolic fraction 89 S3.4. Shared response of Chlorella genotypes to light intensity in the Chlorella metabolic fraction 90 4.1. Weekly growth rates of the native and novel symbioses across the evolution experiment 98 4.2. Growth rate assays performed at multiple points throughout the evolution experiment 99 4.3. Symbiont load at the start and end of the evolution experiment 100 4.4. Fitness of the host-symbiont pairings relative to the symbiont-free host at the start and end of the evolution experiment 101 4.5. The trajectories of the metabolic profiles from the start to the end of the evolution experiment. 103 4.6. Metabolites of interest across the start and end of the evolution experiment within the P. bursaria fraction. 104 4.7. Metabolites of interest across the start and end of the evolution experiment within the Chlorella fraction. 105 7 List of Tables 2.1 15N enriched metabolites of the Chlorella fraction 41 2.2 13C enriched metabolites of the P. bursaria fraction 42 2.3 The identified metabolites of interest from the Chlorella global metabolism. 46 2.4 The identified metabolites of interest from the P. bursaria global metabolism. 49 3.1 Symbiont-genotype specific metabolites in the dark within the 186b P. bursaria host 76 3.2 Symbiont-genotype specific metabolites in the intermediate light within the 186b P. bursaria host 77 3.3 Symbiont-genotype specific metabolites in the high light within the 186b P. bursaria host 78 S3.1 Light-level associated shared Chlorella metabolites across the host and symbiont genotypes. 91 S4.1 Identified metabolites associated with PCA trajectories for the P. bursaria fraction. 110 S4.2 Identified metabolites associated with PCA trajectories for the Chlorella fraction 112 S4.3 Change in symbiont load for each HK1 replicate between the start and end of the evolution experiment 113 8 Acknowledgements First and foremost, I would like to thank my supervisors Michael Brockhurst, Duncan Cameron and A. Jamie Wood for making this project possible and extremely enjoyable. I have learnt a lot over the course of this PhD and it is due to their analytical guidance, which has taught me, among many things, an appreciation of the elegance of good research. I would like to thank Ewan Minter for establishing many of the techniques used in this project and for taking the time to teach these to me. I also wish to thank Chris Lowe for his role in establishing this project and especially for his help while I conducted work in Falmouth. I would like to thank Heather Walker for her technical expertise and help with the mass spectrometry. I am grateful to the BBSRC White Rose DTP program for funding my PhD. To the Brockhurst lab group, thank you for creating a culture that is scientifically exciting, supportive and fun. In particular, thank you to Ellie Harrison and Jamie Hall for your guidance and support. A special thank you to fellow officemates Cagla, Rosanna & Rachael whose friendship I value tremendously. Lastly to my family, Mor, Far & Kim, you have been a constant source of support and inspiration, and thank you for always being willing to listen to how the algae was doing. 9 Declaration I, the author, confirm that the Thesis is my own work. I am aware of the University’s Guidance on the Use of Unfair Means (www.sheffield.ac.uk/ssid/unfair-means). This work has not been previously been presented for an award at this, or any other university. The following publications have arisen from this thesis: • Sørensen, M.E.S., Lowe, C.D., Minter, E.J.A., Wood, A.J., Cameron, D.D., and Brockhurst, M.A.
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